The genome of all organisms is spatially organized to function efficiently. The advent of genome-wide chromatin conformation capture (Hi-C) methods has revolutionized our ability to probe the three-dimensional (3D) organization of genomes across diverse species. In this Review, we compare 3D chromatin folding from bacteria and archaea to that in mammals and plants, focusing on topology at the level of gene regulatory domains. In doing so, we consider systematic similarities and differences that hint at the origin and evolution of spatial chromatin folding and its relation to gene activity. We discuss the universality of spatial chromatin domains in all kingdoms, each encompassing one to several genes. We also highlight differences between organisms and suggest that similar features in Hi-C matrices do not necessarily reflect the same biological process or function. Furthermore, we discuss the evolution of domain boundaries and boundary-forming proteins, which indicates that structural maintenance of chromosome (SMC) proteins and the transcription machinery are the ancestral sculptors of the genome. Architectural proteins such as CTCF serve as clade-specific determinants of genome organization. Finally, studies in many non-model organisms show that, despite the ancient origin of 3D chromatin folding and its intricate link to gene activity, evolution tolerates substantial changes in genome organization.

所有生物体的基因组在空间上都是组织起来的，以有效地发挥作用。全基因组染色质构象捕获 （Hi-C） 方法的出现彻底改变了我们探测不同物种基因组的三维 （3D） 组织的能力。在这篇综述中，我们将细菌和古细菌的 3D 染色质折叠与哺乳动物和植物中的 3D 染色质折叠进行了比较，重点关注基因调控域水平的拓扑结构。在此过程中，我们考虑了暗示空间染色质折叠的起源和进化及其与基因活性的关系的系统相似性和差异性。我们讨论了空间染色质结构域在所有王国中的普遍性，每个王国都包含一到几个基因。我们还强调了生物体之间的差异，并表明 Hi-C 基质中的相似特征不一定反映相同的生物过程或功能。此外，我们讨论了结构域边界和边界形成蛋白的进化，这表明染色体的结构维持 （SMC） 蛋白和转录机制是基因组的祖先雕塑家。结构蛋白（如 CTCF）是基因组组织的进化枝特异性决定因素。最后，对许多非模式生物的研究表明，尽管 3D 染色质折叠起源古老，并且与基因活动有着错综复杂的联系，但进化可以容忍基因组组织的实质性变化。